Involvement of AMPA receptor desensitization in short-term synaptic depression at the calyx of Held in developing rats

Journal of Physiology

Volumn 586, Issue 9, 2008, Pages 2263-2275

  Koike Tani, Maki ^a   Kanda, Takeshi ^a   Saitoh, Naoto ^a,b   Yamashita, Takayuki ^a,c   Takahashi, Tomoyuki ^a,b,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b DOSHISHA UNIVERSITY   (Japan)

^c OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM ION; GLUTAMATE RECEPTOR; MAGNESIUM ION; GLUTAMATE RECEPTOR 1; GLUTAMIC ACID; NEUROTRANSMITTER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTERMETHOD COMPARISON; MOLECULAR MECHANICS; NERVE CELL PLASTICITY; NERVE FUNCTION; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTNATAL DEVELOPMENT; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPTIC TRANSMISSION; BRAIN SLICE; BRAIN STEM; CALYX OF HELD; EXCITATORY POSTSYNAPTIC POTENTIAL; HEARING; NERVOUS SYSTEM PARAMETERS; PAIRED PULSE FACILITATION; PATCH CLAMP TECHNIQUE; POSTSYNAPTIC MEMBRANE; SINGLE CELL ANALYSIS; SYNAPTIC DEPRESSION; TRAPEZOID BODY;

AGING; ANIMALS; BRAIN STEM; CELLS, CULTURED; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; LONG-TERM SYNAPTIC DEPRESSION; NEURAL INHIBITION; RATS; RATS, WISTAR; RECEPTORS, AMPA; SYNAPTIC TRANSMISSION;

EID: 42949101249     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2007.142547     Document Type: Article

References (58)

1. Abbott LF, Varela JA, Sen K & Nelson SB (1997). Synaptic depression and cortical gain control. Science 275, 220-224.
2. Ashby MC, De La Rue SA, Ralph GS, Uney J, Collingridge GL & Henley JM (2004). Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J Neurosci 24, 5172-5176.
3. Barnes-Davies M & Forsythe ID (1995). Pre- and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brain stem slices. J Physiol 488, 387-406.
4. Betz WJ (1970). Depression of transmitter release at the neuromuscular junction of the frog. J Physiol 206, 629-644.
5. Borgdorff AJ & Choquet D (2002). Regulation of AMPA receptor lateral movements. Nature 417, 649-653.
6. Borst JGG, Helmchen F & Sakmann B (1995). Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J Physiol 489, 825-840.
7. Brenowitz S, David J & Trussell L (1998). Enhancement of synaptic efficacy by presynaptic GABA B receptors. Neuron 20, 135-141.
8. Brorson JR, Li D & Suzuki T (2004). Selective expression of heteromeric AMPA receptors driven by flip-flop differences. J Neurosci 24, 3461-3470.
9. Caicedo A & Eybalin M (1999). Glutamate receptor phenotypes in the auditory brainstem and mid-brain of the developing rat. Eur J Neurosci 11, 51-74.
10. Clements JD & Silver RA (2000). Unveiling synaptic plasticity: A new graphical and analytical approach. Trends Neurosci 23, 105-113.
11. DiGregorio DA, Rothman JS, Nielsen TA & Silver RA (2007). Desensitization properties of AMPA receptors at the cerebellar mossy fiber granule cell synapses. J Neurosci 27, 8344-8357.
12. Forsythe ID & Barnes-Davies M (1993). The binaural auditory pathway: membrane currents limiting multiple action potential generation in the rat medial nucleus of the trapezoid body. Proc R Soc Lond Biol Sci 251, 143-150.
13. Foster KA & Regehr WG (2004). Variance-mean analysis in the presence of a rapid antagonist indicates vesicle depletion underlies depression at the climbing fiber synapse. Neuron 43, 119-131.
14. Futai K, Okada M, Matsuyama K & Takahashi T (2001). High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J Neurosci 21, 3342-3349.
15. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193-204.
16. Grosskreutz J, Zoerner A, Schlesinger F, Krampfl K, Dengler R & Bufler J (2003). Kinetic properties of human AMPA-type glutamate receptors expressed in HEK293 cells. Eur J Neurosci 17, 1173-1178.
17. Hermida D, Elezgarai I, Puente N, Alonso V, Anabitarte N, Bilbao A, Doñate-Oliver F & Grandes P (2006). Developmental increase in postsynaptic α-amino-3-hydroxy-5-methyl-4 isoxazolepropionic acid receptor compartmentalization at the calyx of Held synapse. J Comp Neurol 495, 624-634.
18. Huh KH & Wenthold RJ (1999). Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D -aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J Biol Chem 274, 151-157.
19. Ishikawa T, Nakamura Y, Saitoh N, Li WB, Iwasaki S & Takahashi T (2003). Distinct roles of Kv1 and Kv3 potassium channels at the calyx of Held presynaptic terminal. J Neurosci 23, 10445-10453.
20. Ishikawa T & Takahashi T (2001). Mechanisms underlying presynaptic facilitatory effect of cyclothiazide at the calyx of Held of juvenile rats. J Physiol 533, 423-431.
21. Iwasaki S & Takahashi T (2001). Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem. J Physiol 534, 861-871.
22. Joshi I, Shokralla S, Titis P & Wang LY (2004). The role of AMPA receptor gating in the development of high-fidelity neurotransmission at the calyx of Held synapse. J Neurosci 24, 183-196.
23. Joshi I & Wang LY (2002). Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem. J Physiol 540, 861-873.
24. Kandler K & Friauf E (1993). Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol 328, 161-184.
25. Kikuchi K & Hilding D (1965). The development of the organ of Corti in the mouse. Acta Otolaryngol 60, 207-222.
26. Kimura M, Saitoh N & Takahashi T (2003). Adenosine A 1 receptor-mediated presynaptic inhibition at the calyx of Held of immature rats. J Physiol 553, 415-426.
27. Koike M, Tsukada S, Tsuzuki K, Kijima H & Ozawa S (2000). Regulation of kinetic properties of GluR2 AMPA receptor channels by alternative splicing. J Neurosci 20, 2166-2174.
28. Koike-Tani M, Saitoh N & Takahashi T (2005). Mechanisms underlying developmental speeding in AMPA-EPSC decay time at the calyx of Held. J Neurosci 25, 199-207.
29. Krampfl K, Schlesinger F, Zörner A, Kappler M, Dengler R & Bufler J (2002). Control of kinetic properties of GluR2 flop AMPA-type channels: Impact of R/G nuclear editing. Eur J Neurosci 15, 51-62.
30. Kushmerick C, Renden R & von Gersdorff H (2006). Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment. J Neurosci 26, 1366-1377.
31. Lambolez B, Audinat E, Bochet P, Crépel F & Rossier J (1992). AMPA receptor subunits expressed by single Purkinje cells. Neuron 9, 247-258.
32. + channels: Locus, development, and recovery from inactivation at a high-fidelity synapse. J Neurosci 25, 3724-3738.
33. Lomeli H, Mosbacher J, Melcher T, Höger T, Geiger JR, Kuner T, Monyer H, Higuchi M, Bach A & Seeburg PH (1994). Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science 266, 1709-1713.
34. Mammen AL, Huganir RL & O'Brien RJ (1997). Redistribution and stabilization of cell surface glutamate receptors during synapse formation. J Neurosci 17, 7351-7358.
35. Mikaelian D & Ruben RJ (1964). Development of hearing in the normal CBA-J mouse. Acta Otolaryngol 59, 409-422.
36. Nakamura Y & Takahashi T (2007). Developmental changes in potassium currents at the rat calyx of Held presynaptic terminal. J Physiol 581, 1101-1112.
37. Nakamura T, Yamashita T, Saitoh N & Takahashi T (2008). Developmental changes in calcium/calmodulin-dependent inactivation of calcium currents at the calyx of Held. J Physiol.
38. Neher E & Sakaba T (2001). Combining deconvolution and noise analysis for the estimation of transmitter release rates at the calyx of Held. J Neurosci 21, 444-461.
39. Otis T, Zhang S & Trussell LO (1996). Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J Neurosci 16, 7496-7504.
40. Partin KM, Fleck MW & Mayer ML (1996). AMPA receptor flip/flop mutants affecting deactivation, desensitization, and modulation by cyclothiazide, aniracetam, and thiocyanate. J Neurosci 16, 6634-6647.
41. Partin KM, Patneau DK & Mayer ML (1994). Cyclothiazide differentially modulates desensitization of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor splice variants. Mol Pharmacol 46, 129-138.
42. Postlethwaite M, Hennig MH, Steinert JR, Graham BP & Forsythe ID (2007). Acceleration of AMPA receptor kinetics underlies temperature-dependent changes in synaptic strength at the rat calyx of Held. J Physiol 579, 69-84.
43. Quirk JC, Siuda ER & Nisenbaum ES (2004). Molecular determinants responsible for differences in desensitization kinetics of AMPA receptor splice variants. J Neurosci 24, 11416-11420.
44. Renden R, Taschenberger H, Puente N, Rusakov DA, Duvoisin R, Wang LY, Lehre KP & von Gersdorff H (2005). Glutamate transporter studies reveal the pruning of metabotropic glutamate receptors and absence of AMPA receptor desensitization at mature calyx of Held synapses. J Neurosci 25, 8482-8497.
45. Robert A & Howe JR (2003). How AMPA receptor desensitization depends on receptor occupancy. J Neurosci 23, 847-858.
46. Rosenmund C, Stern-Bach Y & Stevens CF (1998). The tetrameric structure of a glutamate receptor channel. Science 280, 1596-1599.
47. Rozov A, Jerecic J, Sakmann B & Burnashev N (2001). AMPA receptor channels with long-lasting desensitization in bipolar interneurons contribute to synaptic depression in a novel feedback circuit in layer 2/ 3 of rat neocortex. J Neurosci 21, 8062-8071.
48. Sätzler K, Söhl LF, Bollmann JH, Borst JG, Frotscher M, Sakmann B & Lübke JH (2002). Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci 22, 10567-10579.
49. Scheuss V, Schneggenburger R & Neher E (2002). Separation of presynaptic and postsynaptic contributions to depression by covariance analysis of successive EPSCs at the calyx of Held synapse. J Neurosci 22, 728-739.
50. Takeuchi N (1958). The effect of temperature on the neuromuscular junction of the frog. Jpn J Physiol 8, 391-404.
51. Taschenberger H, Leão RM, Rowland KC, Spirou GA & von Gersdorff H (2002). Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36, 1127-1143.
52. Taschenberger H, Scheuss V & Neher E (2005). Release kinetics, quantal parameters and their modulation during short-term depression at a developing synapse in the rat CNS. J Physiol 568, 513-537.
53. Taschenberger H & von Gersdorff H (2000). Fine-tuning an auditory synapse for speed and fidelity: Developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20, 9162-9173.
54. Wimmer VC, Horstmann H, Groh A & Kuner T (2006). Donut-like topology of synaptic vesicles with a central cluster of mitochondria wrapped into membrane protrusions: A novel structure-function module of the adult calyx of Held. J Neurosci 109, 109-116.
55. Wong AYC, Graharm BP, Billups B & Forsythe ID (2003). Distinguishing between presynaptic and postsynaptic mechanisms of short-term depression during action potential trains. J Neurosci 23, 4868-4877.
56. Xu J & Wu LG (2005). The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 46, 633-645.
57. 2+ current and its efficacy in triggering transmitter release at the developing calyx of Held synapse. J Neurosci 26, 5698-5708.
58. Zucker RS & Regehr WG (2002). Short-term synaptic plasticity. Annu Rev Physiol 64, 355-405.